Micorrizas y Cambio

8/13/2019 Micorrizas y Cambio

1/9

REVIEW New Phytol. (2000), 147, 179187

Research review

The impact of elevated CO

and global

climate change on arbuscular mycorrhizas:a mycocentric approach

A. H . F I TTE R*, A. H E I N E ME YE R P . L. S TAD D ON

Department of Biology, University of York, PO Box 373, York YO10 5YW, UK

Received 4 November 1999; accepted 6 March 2000

Arbuscular mycorrhizal (AM) symbioses are a potentially important link in the chain of response of ecosystems

to elevated atmospheric [CO]. By promoting plant phosphorus uptake and acting as a sink for plant carbon, they

can alleviate photosynthetic down-regulation. Because hyphal turnover is likely to be fast, especially in warmer

soils, they can also act as a rapid pathway for the return of carbon to the atmosphere. However, most experiments

on AM responses to [CO] have failed to take into account the difference in growth of mycorrhizal and non-

mycorrhizal plants; those that have done so suggest that AM colonization of roots is little altered by [CO],

although this issue remains to be resolved. Very little is known about the effects of other factors of global

environmental change on mycorrhizas. These issues need urgent attention. It is also necessary to understand the

potential for the various AM fungal taxa to respond differentially to environmental changes, including carbon

supply and soil temperature and moisture, especially because of the differential abilities of plant and fungal species

to migrate in response to changing environments. Indeed, there is a need for a new approach to the study of

mycorrhizal associations, which has been too plant-centred. It is essential to regard the fungus as an organism

itself, and to understand its biology both as an entity and as part of a symbiosis.

Key words: elevated [CO], temperature, mycorrhizal function, diversity.

Most (probably 90%; Smith & Read, 1997) plants

form mycorrhizal associations. About two-thirds of

these plants are symbiotic with arbuscular mycor-

rhizal (AM) fungi (Fitter & Moyersoen, 1996).

Except in boreal and some temperate forests and in

heathlands, AM symbiosis is the normal state of the

root systems of most plant species (Read, 1991).

This article concentrates on the AM symbiosis,although many of the arguments apply equally to

other mycorrhizal associations, notably the ecto-

mycorrhizal and ericoid mycorrhizas. However,

these other associations are taxonomically and func-

tionally distinct from the AM symbiosis (Fitter &

Moyersoen, 1996), and it is dangerous to assume that

experimental conclusions obtained from one can be

applied to another.

The fungi involved in AM symbioses are members

of a single order, the Glomales, all of which are

obligate symbionts. Because the AM association

functions on the basis of carbon (C) fixed in

*Author for correspondence (tel 44 1904 432814; fax 44 1904434385; e-mail ahf1york.ac.uk).

photosynthesis moving from plant to fungus, there is

an obvious need to understand what impact an

increasing atmospheric [CO] will have on mycor-

rhizal symbioses. Any such effect is, of course,

indirect as far as the fungus is concerned. The

fungus exists in an environment rich in CO

: both

inside the root and in the soil, [CO] is greater than

current atmospheric [CO]. However, if, for

example, elevated atmospheric [CO] increased the

supply of fixed C to roots, this might promote thegrowth of the fungus. In consequence, services

performed by the fungus might be enhanced, the

best characterized of which is phosphate uptake,

although resistance to drought and pathogens and

increased uptake of other mineral nutrients are also

known to occur (Newsham et al., 1995).

A positive feedback loop can be envisaged, in

which plants respond to elevated [CO] by increased

C fixation followed by the transfer of more carbon

to their root systems ; consequently, mycorrhizal

fungi might grow more and capture more phosphate

(or perform other functions better). The plant would

thus be relieved of a potential deficiency that might

otherwise restrict its ability to respond to elevated


2/9

180 REVIEW A. H. Fitter et al.

AtmosphericCO

2

Respiration Photosynthesis

Leafcarbon

PiandPo

RootcarbonPo

Pi

Plant

Pi

t1/2

>30d

t1/2

>10d

Funguscarbon

t1/2

?

>5d

Pi

Po

Rapid turnover soil C

Slow turnover soil C

Fungus

Soil

Fig. 1. Feedback mechanisms in the response of mycor-

rhizal symbiosis to elevated atmospheric [CO]. Fluxes ofC into and through the biota are shown in red, respirationand decomposition that returns CO

to the atmosphere in

black, and movements of P in blue. Green arrows representcontrols on P movements and transformations by plantand fungal carbohydrate status, and on photosynthesis byleaf P status. Values of t

represent typical or estimated

half-lives of leaves, roots and hyphae that determine ratesof transfer of structural C to the soil organic matter pool.Piand P

orefer to inorganic and organic P; no distinction

is shown between the various components of plant andfungal C pools.

[CO] (Fig. 1), as suggested by the alleviation of

photosynthetic down-regulation (Staddon et al .,1999b). The availability of C for metabolic processes

(Fig. 1) determines key processes in the phosphorus

(P) metabolism of the plant (uptake, transport and

utilization). In return, the P status of the leaf

determines photosynthetic rate. This positive feed-

back is eventually constrained by other deficiencies

(e.g. nitrogen (N) or water), and is therefore only

likely to be important as a control on the processes

shown in Fig. 1 if P is a limiting factor. Nevertheless,

because AM fungi represent an interface in the

soilplant system displayed in Fig. 1, their potential

ability to regulate plant response to global change is

one key reason that their responses need to be

understood.

The other major feature of interest is that

mycorrhizal fungi are a link in the chain of transfers

by which C moves from plant to soil (Staddon et al.,

1999d). They can therefore potentially influence C

cycling rates. Some of the structural C that is

transferred to a symbiotic AM fungus is used to

construct the extraradical mycelium. This network

of fine hyphae almost certainly has a faster turnoverrate than that of either roots or, especially, shoot

material (Fig. 1). This fungal C could therefore be

part of a rapid pathway in the C cycle that returns C

to the atmosphere. By contrast, some fungal com-

pounds might be resistant to microbial attack and

enter a slow pool of recalcitrant soil C, thus

decelerating the cycle (Treseder & Allen, 2000). A

consequence could therefore be the accumulation of

either more or less C in soils. The important

consequences of an increase in atmospheric [CO]

for mycorrhizal functioning could therefore be

changes in the way in which they promote plant

growth andor changes in rates of C cycling. Both of

these are indirect effects, determined by the

responses of plants to [CO], and illustrated by the

top set of connections in Fig. 2. Increased C fixation

can increase C availability to the fungus, thus

promoting fungal ability to provide P to the plant

and improve plant growth. However, other aspects

of climate change might have important direct effects

on AM fungi. If soils warm, the growth of the fungi

might be affected; for example, some fungi might

become active at times of year when they are

currently dormant, or they might respond to dis-

turbance at a different rate. Similarly, changes in soilmoisture content (both drier and wetter conditions

are predicted depending on location, vegetation and

circumstance) would almost certainly have large but

as yet unpredictable effects on AM fungi, as

illustrated by the lower sets of connections in Fig. 2.

However, our understanding of the basic biology of

these organisms is so limited that it is difficult to

make useful predictions about these direct impacts.

In a warmer climate, for example, C fixation by

plants might increase, with the same impacts as

elevated [CO] directly; alternatively, C fixation or

fungal growth might be adversely affected, or theremight be qualitative effects on the structure of the

fungal community or on its temporal pattern (phe-

nology). The wide range of possibilities leads to the

complexity of the potential outcomes of global

change shown in Fig. 2. One important linkage also

shown here is that increased fungal growth, while

promoting P uptake, also increases the C demand by

the fungus, which might act as a regulator on these

interactions.

This article seeks to build on recent advances in

our understanding of the responses of mycorrhizal

associations to environmental change, and to suggest

that a conceptual shift is needed, in which the fungus

itself becomes the focus of experimental investi-


3/9

REVIEW Mycorrhizas and global change 181

CFixation

Plantgrowth

Interface Fungalgrowth

P uptake

C tofungus

C demandby fungus

?

?

?

Changes tofungal taxaphenology

etc.

C tofungus

P uptake

?

Drought

Temp.

[CO2] ?

Fig. 2. Direct and indirect effects of elevated atmospheric [CO] on mycorrhizal fungi. Upward arrows

represent increases, and downward arrows decreases, in the specified processes. Direct effects of soiltemperature and moisture on fungi affect fungal growth and community structure in unknown ways and feedback on the plant community. Indirect effects act through plant C fixation. Both beneficial and deleteriouseffects on plant and fungal growth are potentially self-reinforcing, through positive feedback loops. Regulationof these loops might be achieved via alterations in C demand by the fungus.

gation, rather than the plant alone or even the

symbiosis. We have made no attempt to provide a

comprehensive review of the literature; rather, our

goal is to point to changes in experimental approach

that we believe are needed, highlighting a small

number of recent studies that illuminate this point.

Impact of elevated atmospheric [CO] on AM

colonization

Numerous workers have grown plants at ambient

(usually 350 l l) and elevated (variously 500, 600,

610, 700 and 710 l l) atmospheric [CO] (hereafter

aCO

and eCO

respectively) and have measured the

degree of colonization of the roots by AM fungi

(reviewed by Staddon & Fitter, 1998). Some of thesestudies have been of single plants in pots, and some

have been of whole communities exposed to eCO

in

open-topped chambers or free-air CO

enrichment

(FACE) rings. The results have been inconclusive.

Although decreases in colonization are rarely seen,

increases and null responses are about equally

frequent. In addition, most workers have examined

the morphological structures of the fungi (hyphae,

arbuscules and, where appropriate, vesicles) sep-

arately, and again have reported almost all possible

combinations of increase, decrease and no response.

Staddon & Fitter (1998) argued that this was due to

a serious flaw in such experiments: because eCO

is

known to affect (typically increase) plant growth, if

plants are grown for the same length of time in aCO

and eCO, any comparison between them is of plants

of different sizes and probably different growth

stages. Because the nature and degree of mycorrhizal

colonization of roots are not a plant characteristic,

but are instead highly dependent on plant condition,

consequent changes in colonization would be

expected. Those observed might therefore merely be

artefacts of comparing dissimilar plants (Staddon,

1998).

In a series of time-course experiments, in which a

sequence of harvests allowed the comparison of

plants of similar sizes and developmental stages by

covariance analysis, Staddon and co-workers could

find no evidence that mycorrhizal colonization by an

isolate of Glomus mosseae was affected by growing

plants in eCO

(Fig. 3). This result was true whether

internal (Staddon et al., 1998) or external (Staddonet al., 1999a) colonization was examined and was

robust across a range of 10 different plant species of

contrasting life histories and growth rates (Staddon

et al., 1999c).

There are very few other published studies in

which a proper allometric analysis of mycorrhizal

responses has been made, and it is therefore difficult

to be sure of the generality of these findings. Rouhier

& Read (1998) used three harvests in a study of

Plantago lanceolata ; they found no effect of eCO

at

the first harvest but increases in colonization at the

later two. However, Staddon et al. (1998) showed

that these responses could have been due to growth

effects, which was the conclusion that ONeill et al.


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60

40

20

05 6 7 8 9 10

Loge

plant biomass (mg)

%R

ootlengthcolonized

(a)

(b)7

6

5

4

35 6 7 8 9 10

Logeplant biomass (mg)

Externalmycorrhizalhyphallength

(mmg

1soil)

Fig. 3. The percentage of root length ofPlantago lanceolatacolonized by Glomus mosseae (a) and the external hyphallength (b) are unaffected by growth at elevated (650 l l ;diamonds and broken line) as opposed to ambient (400 l

l

; squares and solid line) [CO], if the effect of [CO] onplant growth is taken into account. Lines are fittedregressions and do not differ between treatments. Data

from Staddonet al. (1999a).

(1991) came to in their three-harvest study of

Liriodendron tulipifera. However, Rillig & Allen

(1999) reported unpublished data that do not

confirm the findings of Staddon and co-workers ,

and Sanderset al. (1998) found a five-fold increase in

extraradical mycelium in eCO

although there was

only a twofold increase in both root biomass and

intraradical mycelium. Until further work has beencompleted, it therefore remains impossible to state

what the likely effects of eCOwill be on mycorrhizal

symbioses. We would urge mycorrhiza researchers

to ensure that they allow for the direct effects of

eCO

on plant growth in all future experiments.

Mechanisms

Because it is certain that the plant must mediate any

effect of eCO

on an AM fungus, we need first to

understand the control of AM colonization. The key

event here is the transfer of C from plant to fungus,

because it is the fungus that is the obligate partner,

and it is that C supply which it cannot obtain

elsewhere. Unfortunately, our knowledge of this

central relationship is poor. It is often assumed that

the arbuscule is the site of both P transfer from

fungus to plant and C transfer from plant to fungus.

Although that assumption is probably correct for P,

it is likely not to be so for C. Histochemical evidence

and the fact that hyphae can colonize roots effectively

even when producing no arbuscules both suggestthat the intercellular hyphae might be at least in part

the location where C is lost from plant cells and is

absorbed by fungal membranes (Smith & Smith,

1996).

If C and P transfer are spatially dislocated, there is

no basis for the assumption that they are meta-

bolically linked. The fungi might merely be effective

scavengers for C that leaks or is exported across plant

cell membranes, able to acquire it in competition

with the reabsorption mechanisms of the plant cells.

The control might therefore be the rate of that loss

from plant cells. It is well established that if plants

are grown under conditions of reduced irradiance or

high P supply, mycorrhizal colonization declines.

This effect is highly variable in terms of the

quantitative relationship between the environmental

factor and the response, but it is nevertheless

qualitatively consistent. The effect of low light is

consistent with a non-specific control mechanism, in

which carbohydrate concentrations control the rate

of efflux from plant cells. The effect of high P could

be explained on the basis that it would increase

metabolic activity, and hence demand for carbo-

hydrate, incidentally reducing efflux. However, such

an explanation should apply equally to N and to P,suggesting a more specific mechanism.

Syvertsen & Graham (1999) conducted a detailed

analysis of the response of two Citrus spp. (Citrus

aurantium and C. sinensis) to eCO

and a high P

supply and, importantly, measured plant carbo-

hydrate pools. High P, eCO

and mycorrhizal

inoculation (with Glomus intraradices) all increased

plant growth, and high P reduced mycorrhizal

colonization; the effect of eCO

on colonization was

weak. All three factors had large impacts on leaf and

root starch concentrations. Leaf starch concen-

trations were low in all P and mycorrhiza treatmentsat aCO

, but greatly increased at eCO

except in non-

mycorrhizal plants at low P. At high P and aCO,

plants had lower root-starch concentrations (Fig. 4).

Mycorrhizal colonization decreased root starch only

at low P and eCO, conditions under which the C

assimilation rate (A) was most stimulated. These

results show that the large C cost imposed by

mycorrhizal colonization on the plant (estimated at

1020% of C fixed in photosynthesis in well

colonized plants) decreases root carbohydrate stores

and stimulates photosynthesis. However, if the effect

is due to mycorrhizal fungi absorbing C that leaks

passively across cell membranes in the root, this does

not necessarily result in an increase in C supply to


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30

20

10

0

(a)

Low P

aCO2

eCO2

aCO2

eCO2

High P

20

10

0

(b)

Low P

aCO2

eCO2

aCO2

eCO2

High P

Fibrousrootstarch

(mgg1)

ACO2

(lmolm2s1)

Fig. 4.(a) Colonization of roots ofCitrus aurantiumby themycorrhizal fungus Glomus intraradices (closed bars)

decreases root starch concentration only at low P supplyrates and principally under elevated (710 l l) [CO

]

compared with ambient [CO] (aCO

: 350l l) and non-

mycorrhizal plants (open bars). (b) The impact ofmycorrhizal colonization on C assimilation rate (A

CO)

exactly mirrors that on root starch, with AM colonizationincreasing A

COat low P and eCO

, suggesting the

alleviation of down-regulation of photosynthesis owing tothe more active root sink. Data from Syvertsen & Graham(1999).

the fungus. It merely shows that root carbohydrate

stores decline as fungi compete effectively with plant

cells for apoplastic sugars, resulting in an export of

leaf carbohydrate and relief of the limitation that leaf

starch imposes on photosynthesis (Fig. 1). An

eventual consequence might be an increased C

supply to the fungus, but this is determined by the

dynamics of sugars in the root apoplast and is not a

necessary consequence of eCO.

However, this result might not be universal: a

study of ectomycorrhizas found no correlation

between root starch and sugar concentrations and

the percentage of fine root tips colonized by

mycorrhizal fungi (Lewis et al., 1994). There is an

urgent need for quantitative studies of C fluxes in

mycorrhizal plants under varying [CO].

Fungal diversity

Much work on mycorrhizas has involved the use of

single isolates of AM fungi, often well known

laboratory organisms such as Glomus mosseae. Rillig

& Allen (1999) highlighted this as a feature of the

series of experiments by Staddon et al. (1998,

1999a,b,c) that suggested that the symbiosis was

largely unresponsive to eCO. The potential for

fungal species to behave differently from each other

has indeed received too little attention, partly

because of the inadequacy of our understanding of

fungal taxonomy. For example, many early papers

on AM function give names for fungal species used

that are impossible to verify. Most laboratories now

use a number of well defined isolates, not all of which

have been identified; increasingly, culture collections

such as INVAM (Bentivenga & Morton, 1994) are

able to supply well characterized cultures and this

might lead to a situation in which it is possible to

make direct comparisons between the work of thevarious active research groups. As yet, however, the

number of taxa involved is unknown, althoughc. 150

have been reliably described, and the ecology and

physiology of most of these are equally obscure. If

they differentiate in respect of their response to

environmental factors, as is likely from ecological

first principles, then changing environmental factors

such as temperature, precipitation or N deposition

might alter fungal communities (Fig. 2).

Some fungi seem very much better at supplying P

to host plants than others (Pearson & Jakobsen,

1993). If improved P acquisition is viewed as themain benefit that plants gain from the symbiosis,

what is it that the other fungi do that keeps them in

the community? There are four main possibilities.

1. They are ineffective mutualists that plants cannot

recognize as such, and so they are able to colonize

plants as extensively as more effective fungi.

2. They are effective mutualists with plant species

other than those that have been studied, giving a

system of specific interactions between plant and

fungal species.

3. They are effective mutualists in conditions other

than those that have been studied: most workersuse standard laboratory or growth-chamber con-

ditions and treated or artificial growth media,

whereas soils are often colder (or occasionally

hotter), wetter (or drier), physically difficult (e.g.

compacted) and more biologically active (both

animals and microorganisms).

4. They perform functions other than P uptake:

fungal taxa that transport P poorly to roots might

be better at protecting them from pathogens or

drought, for example. It is reasonable to imagine

that the fungal attribute that best promotes P

acquisition might be an extensive external my-

celium, whereas that which best provided drought

resistance would be an intense development of

fungal mycelium in the rhizosphere, so binding

roots effectively to soil, and that which best gave

protection against pathogens would be an ex-

tensive internal mycelium. These traits might

therefore be mutually exclusive.

Given this level of uncertainty about the role of

fungal diversity, and with the knowledge that it is

not uncommon to find 10 or more species of AM

fungi in the roots of plants in a single community

(Helgason et al., 1998), it is not surprising that we

cannot predict the consequences of an indirectly

acting environmental variable such as eCO

on the


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120

100

80

60

40

20

0

Glomus intraradices

Glomus entunicatum

Acaulospora denticulata

Scutellospora calospora

ChangeateCO2

(%)

Internal

hyphae

Arbuscules

External

hyphae

Spores

Fig. 5. Growing mycorrhizal plants ofArtemisia tridentataat elevated [CO

] (700 l l) results in distinctive changes

in fungal growth parameters depending on the species of

AM fungus involved. Data are percentage change inmycorrhizal fungal growth (internal and external hyphae,arbuscules and spores) at eCO

compared with aCO

(350

l l). Data from Klironomos et al. (1998).

symbiosis. There is evidence that eCO

affects fungal

taxa differentially. First, it has been shown that eCO

can affect mycorrhizal and non-mycorrhizal fungi

differently (Klironomoset al., 1997). Klironomoset

al. (1998) also showed that mycorrhizal fungi

themselves can respond differently to eCO. They

grew the shrub Artemisia tridentata with four AM

fungi, two species ofGlomus(G. intraradices and G.

etunicatum), Acaulospora denticulata and Scutello-spora calosporain pots of an artificial growth medium

in growth chambers. This was a single harvest-pot

experiment, but eCO

had little effect on plant

growth, so the usual strictures about comparability

are less important. The two Glomus spp. promoted

shoot growth more than did the other two fungi

(there were no non-mycorrhizal controls), but they

promoted root growth only under eCO. The

impacts of eCO

on A. denticulata and S. calospora

are therefore especially interesting, because plants

colonized by them were apparently identical in aCO

and eCO. [CO] had no effect on either the internalmycelium or spore production byA.denticulataand

S. calospora, but did increase external mycelium

production (Fig. 5). By contrast, eCO

had no effect

on the external mycelium of the two Glomus spp.,

but it did increase the frequency of arbuscules and

internal hyphae, and also spore production, albeit on

larger root systems. These results demonstrate that

growing plants in high atmospheric [CO] might

have differential impacts on the fungal taxa with

which they associate, but we are a long way from an

understanding of the functional implications.

Furthermore, the reported effects of eCO

on AM

fungi are strongly influenced by soil nutrient avail-

ability, especially N (Klironomoset al., 1996, 1997).

This led Klironomos et al. (1997) to conclude that

eCO

could significantly alter the community struc-

ture of the plantsoil system towards either a more

mutualistic-closed, mycorrhizal dominated food web

under high [CO] and low N availability, [or] a more

opportunistic-open, saprobepathogen dominated

one under high N availability. N deposition is

another increasingly important component of globalchange, which will have large impacts on AM fungi.

Future studies therefore need to be alert to the

possibility that outcomes can be determined by the

selection of isolates. Generalizations about mycor-

rhizal behaviour need to be based on studies with

multiple taxa.

Our ability to predict the impact of rising atmos-

pheric [CO] on mycorrhizal symbioses is strongly

limited by our poor grasp of the biology of the fungal

partner. The great bulk of research on the symbiosis

has used a limited number of often poorly defined

isolates. Most studies have fallen into one of two

categories: pot experiments with single plants and an

inoculum of the fungus, or field experiments with

natural communities comprising several to many

plant species and an unknown number of largely

unidentified fungi. Both of these approaches have

characteristics that limit their value.

In pot experiments, the soil initially contains no

mycelium, except for those fragments that are added

as inoculum. As the plant grows, so must the fungus,

to create the extraradical mycelium with which itforages in soil. This requires the transfer of large

amounts of C (and possibly other elements) from

plant to fungus, so creating the carbon drain

phenomenon that has been shown repeatedly. Such

experiments therefore represent systems far from

any equilibrium: both plant and fungus are estab-

lishing themselves. The nearest analogous field

system is arable agriculture. In most natural and

many agricultural situations, the plants already exist

and are replacing rather than creating structure, and

this, critically, is also true of the fungus. Estimates of

the quantity of extraradical mycorrhizal myceliumvary widely (Smith & Read, 1997, Table 2.3, p. 66),

but 100 m mof root is a reasonable average. Even

allowing for a difference in radius of 10100-fold

between hyphae and roots, this is a substantial

quantity and most pot experiments must be in a

phase of mycelial development when harvested,

unless they are maintained for a long time. Because

the various fungal taxa have distinct patterns of

extraradical growth, it is unsurprising if they respond

differently to a change in C supply in the roots, but

these responses might be quite different from those

that would be shown by an existing mature my-

celium, for which the C was required largely for

maintenance rather than for growth.


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2

1

0

114 15 16

(a)

(b)1

0

1

2

323 24 25

Rootshoot13C

Root 13C

Fig. 6.Carbon transport into mycorrhizas of plants of the

CgrassCynodon dactylonlinked by a mycorrhzal networkto plants of the C

herbPlantago lanceolata(a) in ambientCO

(380l) and (b) in elevated CO

(610l l). (a) In

aCO, C. dactylon has C of c. 15. More negative

values are due toc transport via mycorrhizal hyphae fromP. lanceolata, which has C of c. 30. Root Crepresent both plant and fungal tissue. The differencebetween root and shoot C signals is linearly related tothe root C, showing that all transported C stays in theroots, even after clipping of the shoots at harvest 1(squares) and the subsequent regrowth of the shootsbefore harvest 2 (triangles). Most C. dactylon plants ataCO

have a fraction of the C in their roots derived from

P. lanceolata. Regression analysis showed that the degreeof movement was a function of mycorrhizal hyphal coloni-

zation of roots. (b) Growing the plants at eCO (in whichtheC. dactylon signal was c. 24 and theP. lanceolatasignal c. 40, due to the different C of the addedCO

) had no effect on C transport. From Fitter et al.

(1998), with permission.

These characteristics of AM fungi mean that

conventional pot experiments are inappropriate for

studies on C budgets, symbiotic effectiveness and

other high-level phenomena, although they might

still be ideal arenas for gaining basic data on fungal

physiology, for example the response to soil tem-

perature. An analogy would be that caged birdsmight be usable for studies of basic physiology but

not of breeding behaviour.

Field experiments suffer from a quite different

problem. Here the fungal mycelia are in place but

their identity is almost always unknown, except in

the most general of senses. Many workers have

identified spores extracted from field soils, but Clapp

et al . (1995) showed that there might be no

correlation between spore collections and the fungi

identified within the roots by DNA-based methods.

At some level this problem might be unimportant. If

the concern is merely to quantify rates of C flux from

roots to soil, or turnover rate of hyphal C in soil

(Rillig & Allen, 1999), the identity of the fungal

species can temporarily be ignored. However, pre-

diction is made difficult if the fungal taxa do not all

respond in the same manner to changing environ-

mental conditions.

Field experiments nevertheless have the great

merit of studying the mature fungus, which com-

prises a mycelium in soil that colonizes a large (and

typically unknown) number of root systems. Fitteretal. (1998) have argued that the behaviour of AM

fungi must be studied from this perspective, on the

basis of an examination of the movement of C

between root systems linked by a common mycor-

rhizal network. Using the stable C isotope C and

mixtures of C

(Plantago lanceolata)a n d C

(Cynodon

dactylon) plants, which discriminate differently

against this isotope in photosynthesis, they found

that as much as 40% (although typically 10%) of

the C in the root system of a plant could be derived

from a neighbouring plant. This C could only have

moved through mycorrhizal hyphae linking the rootsystems. However, the C always stayed in the roots

and was never transported to the shoots, even when

the shoots were cut and made to regrow, using stored

reserves from the roots (Fig. 6). This was strong

evidence that the C remained at all times in fungal

structures. Moreover, the great variation in move-

ment of C between plants was best explained by

variations in fungal structures in the roots, with C

moving into roots with many vesicles and out of

roots predominantly colonized by hyphae. Because

vesicles are thought to be C storage structures and

hyphae could be the sites of C acquisition by the

fungus, this result leads to a view of the fungus as an

organism with its own C dynamics and growth

pattern, transporting C from some parts of its

mycelium and into other parts where it is building

reserves. To test whether plants could control these

C dynamics through variation in C supply in the

roots, Fitter et al. (1998) replicated this experiment

under aCO

and eCO. The increased C supply in

the roots of plants under eCO

did not result in any

greater movement out of those root systems, again

supporting the view that fungal behaviour is more

important than variations in plant nutrition in

determining fungal response.Our viewpoint on mycorrhizas has shifted mark-

edly from one in which the plant alone was studied,

with often detailed measurements of plant per-

formance, and a perfunctory assessment of fungal

colonization, to one in which the pair of organisms is

perceived as an integrated symbiosis. However, as

ONeill et al. (1991) have pointed out and as has

recently been reiterated by Rillig & Allen (1999), this

is itself but a step on the path to a proper viewpoint.

They have argued for a hierarchical framework

incorporating plant host, plant population, plant

community, functional group and ecosystem, so as to

be able to answer questions about nutrient uptake,

the control of plant community structure or C flux in


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ecosystems. However, in such an approach it is still

essential to study the fungus as an organism. It is

essential that we not only recognize the existence of

mycorrhizal fungi, but also study them directly as

complete mycelia, including both the extensive

extraradical phase and the numerous intraradical

elements. This is difficult because a single mycelium

can extend for a considerable distance, but the use ofDNA-based techniques now permits the reliable

identification of fungal genotypes in the field, both in

soil and in roots.

We need to understand how these organisms

respond to changes in their biotic and abiotic

environments. For example, one of the few clear

predictions about global change is that there will be

widespread increases in temperature. To our knowl-

edge, the only published work on the effect of

climate change in a broad sense on arbuscular

mycorrhizas is that of Monzet al. (1994). Although

they provided no data on plant responses to the

altered environmental conditions ([CO], tempera-

ture and precipitation), they did find that an increase

in temperature of 4C above ambient decreased the

percentage root length colonized (RLC) by AM

fungi in Pascopyrum smithii after both 2 and 4 yr.

They also found that increased precipitation altered

RLC in bothP.smithiiandBouteloua gracilisbut not

in a consistent or predictable manner, and that eCO

increased RLC in B. gracilis but not in P. smithii.

There are very few other studies on the effects of

soil temperature on mycorrhizas. Barley was not

colonized by Glomus etunicatum at 10C but was at

15C (Baonet al., 1994). Was this because of effectson the plant or on the fungus? The former seems

more likely, because the mycorrhizal colonization of

roots of bluebells (Hyacinthoides non-scripta) reaches

a peak in a woodland in Yorkshire, UK, in

midwinter, when soil temperatures are 5C

(Merryweather & Fitter, 1995). Nevertheless,

colonization of roots of Plantago lanceolata by

Glomus mosseae (but not extraradical hyphal growth

per unit root length) was greater at 20C than at

12C, even allowing for the effects of temperature on

plant growth (A. Heinemeyer, unpublished; Fig. 7).

Some fungi might be more sensitive to temperaturethan others, offering an axis for niche differentiation

in the fungal community. Such a situation would

also ensure that changes in soil temperature have

profound impacts on the composition of that com-

munity, with consequent effects on the plant popu-

lations.

There is also a clear lack of research on the effects

of other atmospheric pollutants such as NH

and O

on mycorrhizas in general (Cairney & Meharg,

1999). Pe rez-Soba et al. (1995) showed that both

NH

and O

had negative effects on ectomycorrhizal

colonization and that these were not alleviated by

eCO. In practice, however, there will be interactions

between all these components of the changing global

50

40

30

20

10

0 20 40 60 80

(a)

Days after planting

LR

C(%)

25

20

15

10

5

0 0.2 0.4 0.6 0.8 1.0

TotalLR

C(m)

Total plant biomass (g)

(b)

Fig. 7. (a) The percentage of the root growth ofPlantagolanceolatacolonized by the fungus Glomus mosseae (L

RC)

increases more rapidly at 20C (closed diamonds, solidline) than at 12C (open diamonds, broken line). (b) Thetotal length of colonized root in the same experiment ishigher at 20C (closed diamonds, solid line) than at 12C(open diamonds, broken line), irrespective of the effect andtemperature on plant biomass. Lines are best-fitregressions.Data from A. Heinemeyer (unpublished).

environment, and other factors not yet mentioned,

such as habitat fragmentation (the effects of which

will be dependent on the distribution and dispersal

abilities of both plants and fungi). It will be

impossible for researchers to adopt the largely

empirical approach that has so far characterized

much ecological work on mycorrhizas. Rather, we

must develop predictive models based on a proper

understanding of the biology of the organisms

involved, and test the explicit predictions of these

models.

We thank Owen Atkin and Angela Hodge for their

comments on the manuscript. Much of the work reported

here was funded by the Natural Environment Research

Council.

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